Carbon Oxidation State in Microbial Polar Lipids Suggests Adaptation to Hot Spring Temperature and Redox Gradients

The influence of oxidation-reduction (redox) potential on the expression of biomolecules is a topic of ongoing exploration in geobiology. In this study, we investigate the novel possibility that structures and compositions of lipids produced by microbial communities are sensitive to environmental redox conditions. We extracted lipids from microbial biomass collected along the thermal and redox gradients of four alkaline hot springs in Yellowstone National Park (YNP) and investigated patterns in the average oxidation state of carbon (ZC), a metric calculated from the chemical formulae of lipid structures. Carbon in intact polar lipids (IPLs) and their alkyl chains becomes more oxidized (higher ZC) with increasing distance from each of the four hot spring sources. This coincides with decreased water temperature and increased concentrations of oxidized inorganic solutes, such as dissolved oxygen, sulfate, and nitrate. Carbon in IPLs is most reduced (lowest ZC) in the hot, reduced conditions upstream, with abundance-weighted ZC values between −1.68 and −1.56. These values increase gradually downstream to around −1.36 to −1.33 in microbial communities living between 29.0 and 38.1◦C. This near-linear increase in ZC can be attributed to a shift from ether-linked to ester-linked alkyl chains, a decrease in average aliphatic carbons per chain (nC), an increase in average degree of unsaturation per chain (nUnsat), and increased cyclization in tetraether lipids. The ZC of lipid headgroups and backbones did not change significantly downstream. Expression of lipids with relatively reduced carbon under reduced conditions and oxidized lipids under oxidized conditions may indicate microbial adaptation across environmental gradients in temperature and electron donor/acceptor supply

Quantifying the effects of hydrogen on carbon assimilation in a seafloor microbial community associated with ultramafic rocks

Thermodynamic models predict that H2 is energetically favorable for seafloor microbial life, but how H2 affects anabolic processes in seafloor-associated communities is poorly understood. Here, we used quantitative 13C DNA stable isotope probing (qSIP) to quantify the effect of H2 on carbon assimilation by microbial taxa synthesizing 13C-labeled DNA that are associated with partially serpentinized peridotite rocks from the equatorial Mid-Atlantic Ridge. The rock-hosted seafloor community was an order of magnitude more diverse compared to the seawater community directly above the rocks. With added H2, peridotite-associated taxa increased assimilation of 13C-bicarbonate and 13C-acetate into 16S rRNA genes of operational taxonomic units by 146% (±29%) and 55% (±34%), respectively, which correlated with enrichment of H2-oxidizing NiFe-hydrogenases encoded in peridotite-associated metagenomes. The effect of H2 on anabolism was phylogenetically organized, with taxa affiliated with Atribacteria, Nitrospira, and Thaumarchaeota exhibiting the most significant increases in 13C-substrate assimilation in the presence of H2. In SIP incubations with added H2, an order of magnitude higher number of peridotite rock-associated taxa assimilated 13C-bicarbonate, 13C-acetate, and 13C-formate compared to taxa that were not associated with peridotites. Collectively, these findings indicate that the unique geochemical nature of the peridotite-hosted ecosystem has selected for H2-metabolizing, rock-associated taxa that can increase anabolism under high H2 concentrations. Because ultramafic rocks are widespread in slow-, and ultraslow-spreading oceanic lithosphere, continental margins, and subduction zones where H2 is formed in copious amounts, the link between H2 and carbon assimilation demonstrated here may be widespread within these geological settings

Influence of Early Low-Temperature and Later High-Temperature Diagenesis on Magnetic Mineral Assemblages in Marine Sediments From the Nankai Trough

Funding Information: This research used samples and data provided by the International Ocean Discovery Program (IODP). The authors thank the Marine Works Japan staff at the Kochi Core Center for support during sampling. This work was supported by the Japan Society for the Promotion of Science Grant-in-Aid for Science Research (grant 17K05681 to Myriam Kars), the German Research Foundation (DFG grants 388260220 to Male Koster and Susann Henkel, and 408178672 to Florence Schubotz), and the Australian Research Council (grant DP200100765 to Andrew P. Roberts). The authors also thank two anonymous reviewers for their constructive comments and Editor Joshua Feinberg for handling the manuscript.Peer reviewedPublisher PD

Fossil organic carbon utilization in marine Arctic fjord sediments by subsurface micro-organisms

Rock-derived or petrogenic organic carbon has traditionally been regarded as being non-bioavailable and bypassing the active carbon cycle when eroded. However, it has become apparent that this organic carbon might not be so inert, especially in fjord systems where petrogenic organic carbon influxes can be high, making its degradation another potential source of greenhouse gas emissions. The extent to which subsurface micro-organisms use this organic carbon is not well constrained, despite its potential impacts on global carbon cycling. Here, we performed compound-specific radiocarbon analyses on intact polar lipid–fatty acids of live micro-organisms from marine sediments in Hornsund Fjord, Svalbard. By this means, we estimate that local bacterial communities utilize between 5 ± 2% and 55 ± 6% (average of 25 ± 16%) of petrogenic organic carbon for their biosynthesis, providing evidence for the important role of petrogenic organic carbon as a substrate after sediment redeposition. We hypothesize that the lack of sufficient recently synthesized organic carbon from primary production forces micro-organisms into utilization of petrogenic organic carbon as an alternative energy source. The input of petrogenic organic carbon to marine sediments and subsequent utilization by subsurface micro-organisms represents a natural source of fossil greenhouse gas emissions over geological timescale

Soothsaying DOM: A Current Perspective on the Future of Oceanic Dissolved Organic Carbon

The vast majority of freshly produced oceanic dissolved organic carbon (DOC) is derived from marine phytoplankton, then rapidly recycled by heterotrophic microbes. A small fraction of this DOC survives long enough to be routed to the interior ocean, which houses the largest and oldest DOC reservoir. DOC reactivity depends upon its intrinsic chemical composition and extrinsic environmental conditions. Therefore, recalcitrance is an emergent property of DOC that is analytically difficult to constrain. New isotopic techniques that track the flow of carbon through individual organic molecules show promise in unveiling specific biosynthetic or degradation pathways that control the metabolic turnover of DOC and its accumulation in the deep ocean. However, a multivariate approach is required to constrain current carbon fluxes so that we may better predict how the cycling of oceanic DOC will be altered with continued climate change. Ocean warming, acidification, and oxygen depletion may upset the balance between the primary production and heterotrophic reworking of DOC, thus modifying the amount and/or composition of recalcitrant DOC. Climate change and anthropogenic activities may enhance mobilization of terrestrial DOC and/or stimulate DOC production in coastal waters, but it is unclear how this would affect the flux of DOC to the open ocean. Here, we assess current knowledge on the oceanic DOC cycle and identify research gaps that must be addressed to successfully implement its use in global scale carbon models

Hot fluids, burial metamorphism and thermal histories in the underthrust sediments at IODP 370 site C0023, Nankai Accretionary Complex

This research used samples and data provided by the International Ocean Discovery Program (IODP). The authors are grateful to the IODP and the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT). We thank crew, drilling team, geologists and lab technicians on D/V Chikyu and the staff of the Kochi Institute for Core Sample Research for supporting operations. This work was supported by the ECORD research grant [2017 to MYT]; and the NERC grant [NE/P015182/1 2017 to SAB]. ZW acknowledges technical support provided by Colin Taylor at the University of Aberdeen. Petromod 2017 was provided by Schlumberger. VBH and KUH acknowledge funding from the Deutsche Forschungsgemeinschaft through the Cluster of Excellence, The Ocean Floor – Earth’s Uncharted Interface“ and Project Grant HE8034/1-1 2019. This is a contribution to the Deep Carbon Observatory.Peer reviewedPublisher PD

Environmental micro-niche filtering shapes bacterial pioneer communities during primary colonization of a Himalayas' glacier forefield

The pedogenesis from the mineral substrate released upon glacier melting has been explained with the succession of consortia of pioneer microorganisms, whose structure and functionality are determined by the environmental conditions developing in the moraine. However, the microbiome variability that can be expected in the environmentally heterogeneous niches occurring in a moraine at a given successional stage is poorly investigated. In a 50 m2 area in the forefield of the Lobuche glacier (Himalayas, 5050 m above sea level), we studied six sites of primary colonization presenting different topographical features (orientation, elevation and slope) and harbouring greyish/dark biological soil crusts (BSCs). The spatial vicinity of the sites opposed to their topographical differences, allowed us to examine the effect of environmental conditions independently from the time of deglaciation. The bacterial microbiome diversity and their co-occurrence network, the bacterial metabolisms predicted from 16S rRNA gene high-throughput sequencing, and the microbiome intact polar lipids were investigated in the BSCs and the underlying sediment deep layers (DLs). Different bacterial microbiomes inhabited the BSCs and the DLs, and their composition varied among sites, indicating a niche-specific role of the micro-environmental conditions in the bacterial communities' assembly. In the heterogeneous sediments of glacier moraines, physico-chemical and micro-climatic variations at the site-spatial scale are crucial in shaping the microbiome microvariability and structuring the pioneer bacterial communities during pedogenesis

Massive asphalt deposits, oil seepage, and gas venting support abundant chemosynthetic communities at the Campeche Knolls, southern Gulf of Mexico

Hydrocarbon seepage is a widespread process at the continental margins of the Gulf of Mexico. We used a multidisciplinary approach, including multibeam mapping and visual seafloor observations with different underwater vehicles to study the extent and character of complex hydrocarbon seepage in the Bay of Campeche, southern Gulf of Mexico. Our observations showed that seafloor asphalt deposits previously only known from the Chapopote Knoll also occur at numerous other knolls and ridges in water depths from 1230 to 3150 m. In particular the deeper sites (Chapopopte and Mictlan knolls) were characterized by asphalt deposits accompanied by extrusion of liquid oil in form of whips or sheets, and in some places (Tsanyao Yang, Mictlan, and Chapopote knolls) by gas emission and the presence of gas hydrates in addition. Molecular and stable carbon isotopic compositions of gaseous hydrocarbons suggest their primarily thermogenic origin. Relatively fresh asphalt structures were settled by chemosynthetic communities including bacterial mats and vestimentiferan tube worms, whereas older flows appeared largely inert and devoid of corals and anemones at the deep sites. The gas hydrates at Tsanyao Yang and Mictlan Knolls were covered by a 5-to-10 cm-thick reaction zone composed of authigenic carbonates, detritus, and microbial mats, and were densely colonized by 1–2 m-long tube worms, bivalves, snails, and shrimps. This study increased knowledge on the occurrences and dimensions of asphalt fields and associated gas hydrates at the Campeche Knolls. The extent of all discovered seepage structure areas indicates that emission of complex hydrocarbons is a widespread, thus important feature of the southern Gulf of Mexico

In-situ mechanical weakness of subducting sediments beneath a plate boundary décollement in the Nankai Trough

© 2018, The Author(s). The study investigates the in-situ strength of sediments across a plate boundary décollement using drilling parameters recorded when a 1180-m-deep borehole was established during International Ocean Discovery Program (IODP) Expedition 370, Temperature-Limit of the Deep Biosphere off Muroto (T-Limit). Information of the in-situ strength of the shallow portion in/around a plate boundary fault zone is critical for understanding the development of accretionary prisms and of the décollement itself. Studies using seismic reflection surveys and scientific ocean drillings have recently revealed the existence of high pore pressure zones around frontal accretionary prisms, which may reduce the effective strength of the sediments. A direct measurement of in-situ strength by experiments, however, has not been executed due to the difficulty in estimating in-situ stress conditions. In this study, we derived a depth profile for the in-situ strength of a frontal accretionary prism across a décollement from drilling parameters using the recently established equivalent strength (EST) method. At site C0023, the toe of the accretionary prism area off Cape Muroto, Japan, the EST gradually increases with depth but undergoes a sudden change at ~ 800 mbsf, corresponding to the top of the subducting sediment. At this depth, directly below the décollement zone, the EST decreases from ~ 10 to 2 MPa, with a change in the baseline. This mechanically weak zone in the subducting sediments extends over 250 m (~ 800–1050 mbsf), corresponding to the zone where the fluid influx was discovered, and high-fluid pressure was suggested by previous seismic imaging observations. Although the origin of the fluids or absolute values of the strength remain unclear, our investigations support previous studies suggesting that elevated pore pressure beneath the décollement weakens the subducting sediments. [Figure not available: see fulltext.]

Microbial community characterization and carbon turnover in methane-rich environments - case studies in the Gulf of Mexico and the Black Sea

This thesis investigated patterns in the distribution of intact polar membrane lipids (IPLs) in the marine environment. IPL analysis is a relatively new tool in microbial ecology to study (i) live microbial biomass and (ii) the dominating microbial players. This technique was applied for the first time to study the oxic and anoxic water column of the Black Sea and observed a stratification of IPLs according to geochemical zonation. Export of IPLs to the sediment was found to be selective and the distribution of IPLs in the upper 2 cm of the sediments reflects de novo production of IPLs by indigenous microbes, putatively identified as sulfate-reducing bacteria and benthic archaea. The distribution of archaeal IPLs in the anoxic water body did not indicate the abundant presence of methanotrophic archaea, which were presumed in earlier studies due to high estimated methane oxidation rates. The presence of betaine lipids and glycosidic sphingolipids in the anoxic water column could be linked to unknown anaerobic bacteria and is a novel finding as these lipids are primarily known to be produced by eukaryotes.Investigations of microbial communities associated to the Chapopote asphalt seep in the southern Gulf of Mexico revealed the presence of a diverse array of IPLs from both Bacteria and Archaea. IPL concentrations in the sediments were correlated with the abundant presence of oil and methane, indicating that the petroleum hydrocarbons are a major stimulant for microbial activity. Bacterial IPL concentrations decreased with decreasing sulfate concentrations over depth, whereas archaeal IPLs increased simultaneously and comprised up to 80% of total IPLs at ca. 15 cm sediment depth. Bacterial lipids mainly included phospholipids with the polar head groups phosphatidylethanolamine (PE), phosphatidyl-(N)-methylethanolamine (PME), and phosphatidylglycerol (PG). The assignment of these IPLs to sulfate-reducing bacteria (SRB) was confirmed by the presence of SRB-characteristic fatty acids. Polar head group-specific isotope analysis of the SRB core lipids revealed that the majority of the SRB population is autotrophic and involved in the anaerobic oxidation of methane. However, a large amount of SRB are heterotrophic hydrocarbon-degrading bacteria. The oil-degrading bacteria mainly contained PME as head group. Archaeal IPLs indicated the presence of ANME-1 archaea comprised of diglycosidic glyceroldibiphytanylglyceroltetraethers (2Gly-GDGT) accompanied by ANME-2 archaea suggested by phosphate-based hydroxyarchaeols. Polar head group-specific stable carbon isotope analysis of the archaeal IPLs confirmed the association of those lipids to methanotrophic archaea and could also show that phosphate-based archaeols and GDGTs with mixed glycosidic and phosphate-based head groups were mainly derived from methanogenic archaea. In subsurface sediments of the oil-influenced Chapopote asphalt seep abundant archaeal IPLs were detected close to a sulfate-methane transition zone. Here, bacterial lipids were only a minor part of the total IPLs and were dominated by diether lipids with PE headgroups. Phosphate-based hydroxyarchaeols and diglycosidic GDGTs could be assigned to both methanogenic and methanotrophic sources. Methane is thus a major intermediate in microbial metabolism at the Chapopote asphalt volcano. Investigations of biological and physical weathering of the deposited asphalts showedthat the asphalts are an important substrate for the microbial community. The removal of n-alkanes, branched alkanes, isoprenoids and low molecular weight polyaromatic hydrocarbon compounds could be primarily assigned to biodegradation. Biomarkers such as steranes and hopanes were most recalcitrant and were still observed in highly weathered brittle asphalts. Comparison of fresh and weathered asphalts allowed to estimate total petroleum hydrocarbon losses into the environment. Assessment of the potential of total hydrocarbon emission from the Chapopote asphalt seep amounts to up to 1,540 Ã ± 770 tons. However, there is indication that a large fraction of these hydrocarbons are already efficiently recycled by the indigenous microorganisms associated to the asphalts